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Transcriptome analysis of the Populus trichocarpa-Rhizophagus irregularis Mycorrhizal Symbiosis: Regulation of Plant and Fungal Transportomes under Nitrogen Starvation.

Identifieur interne : 001142 ( Main/Exploration ); précédent : 001141; suivant : 001143

Transcriptome analysis of the Populus trichocarpa-Rhizophagus irregularis Mycorrhizal Symbiosis: Regulation of Plant and Fungal Transportomes under Nitrogen Starvation.

Auteurs : Silvia Calabrese [Suisse] ; Annegret Kohler [France] ; Annette Niehl [Suisse] ; Claire Veneault-Fourrey [France] ; Thomas Boller [Suisse] ; Pierre-Emmanuel Courty [Suisse, France]

Source :

RBID : pubmed:28387868

Descripteurs français

English descriptors

Abstract

Nutrient transfer is a key feature of the arbuscular mycorrhizal (AM) symbiosis. Valuable mineral nutrients are transferred from the AM fungus to the plant, increasing its fitness and productivity, and, in exchange, the AM fungus receives carbohydrates as an energy source from the plant. Here, we analyzed the transcriptome of the Populus trichocarpa-Rhizophagus irregularis symbiosis using RNA-sequencing of non-mycorrhizal or mycorrhizal fine roots, with a focus on the effect of nitrogen (N) starvation. In R. irregularis, we identified 1,015 differentially expressed genes, whereby N starvation led to a general induction of gene expression. Genes of the functional classes of cell growth, membrane biogenesis and cell structural components were highly abundant. Interestingly, N starvation also led to a general induction of fungal transporters, indicating increased nutrient demand upon N starvation. In non-mycorrhizal P. trichocarpa roots, 1,341 genes were differentially expressed under N starvation. Among the 953 down-regulated genes in N starvation, most were involved in metabolic processes including amino acids, carbohydrate and inorganic ion transport, while the 342 up-regulated genes included many defense-related genes. Mycorrhization led to the up-regulation of 549 genes mainly involved in secondary metabolite biosynthesis and transport; only 24 genes were down-regulated. Mycorrhization specifically induced expression of three ammonium transporters and one phosphate transporter, independently of the N conditions, corroborating the hypothesis that these transporters are important for symbiotic nutrient exchange. In conclusion, our data establish a framework of gene expression in the two symbiotic partners under high-N and low-N conditions.

DOI: 10.1093/pcp/pcx044
PubMed: 28387868


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<term>Gene Expression Profiling (MeSH)</term>
<term>Gene Expression Regulation, Plant (genetics)</term>
<term>Mycorrhizae (physiology)</term>
<term>Nitrogen (metabolism)</term>
<term>Plant Proteins (genetics)</term>
<term>Plant Proteins (metabolism)</term>
<term>Populus (genetics)</term>
<term>Populus (microbiology)</term>
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<term>Analyse de profil d'expression de gènes (MeSH)</term>
<term>Azote (métabolisme)</term>
<term>Mycorhizes (physiologie)</term>
<term>Populus (génétique)</term>
<term>Populus (microbiologie)</term>
<term>Protéines végétales (génétique)</term>
<term>Protéines végétales (métabolisme)</term>
<term>Régulation de l'expression des gènes végétaux (génétique)</term>
<term>Symbiose (génétique)</term>
<term>Symbiose (physiologie)</term>
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<term>Plant Proteins</term>
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<term>Régulation de l'expression des gènes végétaux</term>
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<div type="abstract" xml:lang="en">Nutrient transfer is a key feature of the arbuscular mycorrhizal (AM) symbiosis. Valuable mineral nutrients are transferred from the AM fungus to the plant, increasing its fitness and productivity, and, in exchange, the AM fungus receives carbohydrates as an energy source from the plant. Here, we analyzed the transcriptome of the Populus trichocarpa-Rhizophagus irregularis symbiosis using RNA-sequencing of non-mycorrhizal or mycorrhizal fine roots, with a focus on the effect of nitrogen (N) starvation. In R. irregularis, we identified 1,015 differentially expressed genes, whereby N starvation led to a general induction of gene expression. Genes of the functional classes of cell growth, membrane biogenesis and cell structural components were highly abundant. Interestingly, N starvation also led to a general induction of fungal transporters, indicating increased nutrient demand upon N starvation. In non-mycorrhizal P. trichocarpa roots, 1,341 genes were differentially expressed under N starvation. Among the 953 down-regulated genes in N starvation, most were involved in metabolic processes including amino acids, carbohydrate and inorganic ion transport, while the 342 up-regulated genes included many defense-related genes. Mycorrhization led to the up-regulation of 549 genes mainly involved in secondary metabolite biosynthesis and transport; only 24 genes were down-regulated. Mycorrhization specifically induced expression of three ammonium transporters and one phosphate transporter, independently of the N conditions, corroborating the hypothesis that these transporters are important for symbiotic nutrient exchange. In conclusion, our data establish a framework of gene expression in the two symbiotic partners under high-N and low-N conditions.</div>
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<AbstractText>Nutrient transfer is a key feature of the arbuscular mycorrhizal (AM) symbiosis. Valuable mineral nutrients are transferred from the AM fungus to the plant, increasing its fitness and productivity, and, in exchange, the AM fungus receives carbohydrates as an energy source from the plant. Here, we analyzed the transcriptome of the Populus trichocarpa-Rhizophagus irregularis symbiosis using RNA-sequencing of non-mycorrhizal or mycorrhizal fine roots, with a focus on the effect of nitrogen (N) starvation. In R. irregularis, we identified 1,015 differentially expressed genes, whereby N starvation led to a general induction of gene expression. Genes of the functional classes of cell growth, membrane biogenesis and cell structural components were highly abundant. Interestingly, N starvation also led to a general induction of fungal transporters, indicating increased nutrient demand upon N starvation. In non-mycorrhizal P. trichocarpa roots, 1,341 genes were differentially expressed under N starvation. Among the 953 down-regulated genes in N starvation, most were involved in metabolic processes including amino acids, carbohydrate and inorganic ion transport, while the 342 up-regulated genes included many defense-related genes. Mycorrhization led to the up-regulation of 549 genes mainly involved in secondary metabolite biosynthesis and transport; only 24 genes were down-regulated. Mycorrhization specifically induced expression of three ammonium transporters and one phosphate transporter, independently of the N conditions, corroborating the hypothesis that these transporters are important for symbiotic nutrient exchange. In conclusion, our data establish a framework of gene expression in the two symbiotic partners under high-N and low-N conditions.</AbstractText>
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<Country>Japan</Country>
<MedlineTA>Plant Cell Physiol</MedlineTA>
<NlmUniqueID>9430925</NlmUniqueID>
<ISSNLinking>0032-0781</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D010940">Plant Proteins</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>N762921K75</RegistryNumber>
<NameOfSubstance UI="D009584">Nitrogen</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D020869" MajorTopicYN="Y">Gene Expression Profiling</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018506" MajorTopicYN="N">Gene Expression Regulation, Plant</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D038821" MajorTopicYN="N">Mycorrhizae</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D009584" MajorTopicYN="N">Nitrogen</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D010940" MajorTopicYN="N">Plant Proteins</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D032107" MajorTopicYN="N">Populus</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013559" MajorTopicYN="N">Symbiosis</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000502" MajorTopicYN="N">physiology</QualifierName>
</MeshHeading>
</MeshHeadingList>
<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="Y">Ammonium transporter</Keyword>
<Keyword MajorTopicYN="Y">Arbuscular mycorrhiza</Keyword>
<Keyword MajorTopicYN="Y">Nitrogen metabolism</Keyword>
<Keyword MajorTopicYN="Y">Populus trichocarpa</Keyword>
<Keyword MajorTopicYN="Y">Rhizophagus irregularis</Keyword>
<Keyword MajorTopicYN="Y">Symbiosis</Keyword>
<Keyword MajorTopicYN="Y">Transcriptome</Keyword>
<Keyword MajorTopicYN="Y">Transportome</Keyword>
</KeywordList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2016</Year>
<Month>02</Month>
<Day>15</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2017</Year>
<Month>03</Month>
<Day>17</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2017</Year>
<Month>4</Month>
<Day>8</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="medline">
<Year>2017</Year>
<Month>11</Month>
<Day>29</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2017</Year>
<Month>4</Month>
<Day>8</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">28387868</ArticleId>
<ArticleId IdType="pii">3109098</ArticleId>
<ArticleId IdType="doi">10.1093/pcp/pcx044</ArticleId>
</ArticleIdList>
</PubmedData>
</pubmed>
<affiliations>
<list>
<country>
<li>France</li>
<li>Suisse</li>
</country>
<region>
<li>Bourgogne</li>
<li>Bourgogne-Franche-Comté</li>
<li>Grand Est</li>
<li>Lorraine (région)</li>
</region>
<settlement>
<li>Champenoux</li>
<li>Dijon</li>
<li>Nancy</li>
<li>Vandœuvre-lès-Nancy</li>
</settlement>
<orgName>
<li>Université de Lorraine</li>
</orgName>
</list>
<tree>
<country name="Suisse">
<noRegion>
<name sortKey="Calabrese, Silvia" sort="Calabrese, Silvia" uniqKey="Calabrese S" first="Silvia" last="Calabrese">Silvia Calabrese</name>
</noRegion>
<name sortKey="Boller, Thomas" sort="Boller, Thomas" uniqKey="Boller T" first="Thomas" last="Boller">Thomas Boller</name>
<name sortKey="Courty, Pierre Emmanuel" sort="Courty, Pierre Emmanuel" uniqKey="Courty P" first="Pierre-Emmanuel" last="Courty">Pierre-Emmanuel Courty</name>
<name sortKey="Niehl, Annette" sort="Niehl, Annette" uniqKey="Niehl A" first="Annette" last="Niehl">Annette Niehl</name>
</country>
<country name="France">
<region name="Grand Est">
<name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name>
</region>
<name sortKey="Courty, Pierre Emmanuel" sort="Courty, Pierre Emmanuel" uniqKey="Courty P" first="Pierre-Emmanuel" last="Courty">Pierre-Emmanuel Courty</name>
<name sortKey="Kohler, Annegret" sort="Kohler, Annegret" uniqKey="Kohler A" first="Annegret" last="Kohler">Annegret Kohler</name>
<name sortKey="Veneault Fourrey, Claire" sort="Veneault Fourrey, Claire" uniqKey="Veneault Fourrey C" first="Claire" last="Veneault-Fourrey">Claire Veneault-Fourrey</name>
<name sortKey="Veneault Fourrey, Claire" sort="Veneault Fourrey, Claire" uniqKey="Veneault Fourrey C" first="Claire" last="Veneault-Fourrey">Claire Veneault-Fourrey</name>
</country>
</tree>
</affiliations>
</record>

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